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Salzman Cycads 2020.Pdf SCIENCE ADVANCES | RESEARCH ARTICLE ORGANISMAL BIOLOGY Copyright © 2020 The Authors, some rights reserved; An ancient push-pull pollination mechanism in cycads exclusive licensee Shayla Salzman1,2,3*†, Damon Crook4, James D. Crall1, Robin Hopkins1,2‡, Naomi E. Pierce1,3‡ American Association for the Advancement of Science. No claim to Most cycads engage in brood-site pollination mutualisms, yet the mechanism by which the Cycadales entice original U.S. Government pollination services from diverse insect mutualists remains unknown. Here, we characterize a push-pull pollina- Works. Distributed tion mechanism between a New World cycad and its weevil pollinators that mirrors the mechanism between a under a Creative distantly related Old World cycad and its thrips pollinators. The behavioral convergence between weevils and Commons Attribution thrips, combined with molecular phylogenetic dating and a meta-analysis of thermogenesis and coordinated patterns NonCommercial of volatile attraction and repulsion suggest that a push-pull pollination mutualism strategy is ancestral in this License 4.0 (CC BY-NC). ancient, dioecious plant group. Hence, it may represent one of the earliest insect/plant pollination mechanisms, arising long before the evolution of visual floral signaling commonly used by flowering plants. INTRODUCTION brood-site mutualist is repelled from its host pollen cone and en- Downloaded from Highly specialized coevolved systems are uncommon in nature and ticed into ovulate cones has been described in M. lucida (5), where are sometimes considered evolutionary dead ends (1). However, the Cycadothrips chadwickii thrips (order: Thysanoptera) are attracted plant order Cycadales is one of the oldest living lineages of seed (“pulled”) by lower concentrations of the dominant plant volatile plants (2), and most species form obligate brood-site pollination compound, b-myrcene, and repelled (“pushed”) by higher concen- mutualisms with insects (3, 4). Here, we investigate whether unre- trations of the same compound. The daily plant thermogenic and lated pollination mutualists exhibit matching behavioral responses volatile cycle induces pollinator movement between pollen and http://advances.sciencemag.org/ to conserved plant behaviors, representing a shared pollination ovulate cones, enabling pollination and seed set (5). This push-pull strategy. The push-pull pollination mechanism of the Australian pollination mechanism differs from most pollination syndromes cycad Macrozamia lucida is characterized by a daily peak in plant because it has a repulsive component that expels pollinators from thermogenesis and volatile production whereby thrips pollination pollen cones at a certain point in the cycle in addition to the attrac- mutualists are attracted to lower levels of a plant volatile and repelled tive mechanisms commonly seen in the visual and chemical cues of by high levels of the same compound (5). Across the Cycadales, flowers. Furthermore, the same chemical cue is used for attraction pollination-stage cones undergo a daily cycle of thermogenesis (6) and repulsion. and respiratory processes that similarly culminate in a peak of vola- The Mexican cycad Zamia furfuracea (Zamiacea), which is more tile production (7). By analyzing a distantly related New World than 150 million years (Ma) diverged from M. lucida, has an obligate cycad species that, like most cycads, is associated with a coleopteran pollination mutualism with Rhopalotria furfuracea (Coleoptera: pollination mutualist, we investigate whether this characteristic Belidae) weevils (formally R. mollis) (17). R. furfuracea complete on September 14, 2020 cycle of thermogenesis and coordinated volatile production is broadly their entire development within the plants’ disposable pollen cone indicative of an ancient and conserved pollination strategy. parenchyma tissue (10), and the plants do not set seed without Within the dioecious Cycadales, specialized insect pollinators, pollinators (17). Specialized coleopteran pollination is widespread mostly beetles and weevils, live and feed almost exclusively within in extant Cycadales (3, 4) and has existed in the lineage since at least the male pollen cone tissue (3, 4, 8–10), although one obligate ovule the mid-Mesozoic where fossilized Boganiidae beetle pollinators parasite may play a minor role in pollination of Encephalartos villosus have been found (18) well before the rise of flowering plants (19) or (9). Successful cycad reproduction requires these brood-site mutu- the earliest known direct evidence of thrips pollination (20). While alists to leave the host pollen cone and transfer pollen to a female push-pull pollination has also been hypothesized for Coleoptera- ovulate cone. Over the course of a day, pollination-stage cones pro- pollinated cycads (21, 22), the mechanism by which the plants duce a predictable thermogenic and volatile pattern (7). Both pollen manipulate their behavior to carry out pollination has not yet been and ovulate cones of an individual species produce similar thermo- explored. genic and volatile profiles (6, 11–14), yet across all species, pollen cones produce higher temperature peaks (6) and more concentrated volatile compounds (3, 11, 12, 14). Pollinator exit from pollen cones RESULTS has been observed to coincide with thermogenic and volatile peaks Plant volatile profile and weevil physiological response (5, 12, 15–17). The specific behavioral mechanism by which a We identify the chemical communication mechanism underlying the mutualism between R. furfuracea and Z. furfuracea. Using head- space collection methods, plant volatile compounds were collected 1 Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford from Z. furfuracea pollen (n = 8) and ovulate cones (n = 7) to deter- Street, Cambridge, MA 02138, USA. 2The Arnold Arboretum, Harvard University, Boston, MA 02131, USA. 3Museum of Comparative Zoology, Harvard University, 26 mine the plant volatile profile and the physiological response of Oxford Street, Cambridge, MA 02138, USA. 4USDA-APHIS-PPQ CPHST, Otis Laboratory, R. furfuracea to host plant volatiles. Z. furfuracea pollen and ovulate Building 1398, Otis ANGB, MA 02542, USA. cones produce two major compounds: the hydrocarbon 1,3-octadiene *Corresponding author. Email: [email protected] and the alcohol linalool (Fig. 1). Electroantenograph detection †Present address: School of Integrative Plant Sciences, Section of Plant Biology, Cornell University, 502 Mann Library, Ithaca, NY 14853, USA. (EAD) demonstrated that R. furfuracea male and female weevils are ‡These authors share senior authorship. physiologically capable of perceiving only 1,3-octadiene (n = 10; Salzman et al., Sci. Adv. 2020; 6 : eaay6169 12 June 2020 1 of 9 SCIENCE ADVANCES | RESEARCH ARTICLE A 0.6 0.4 vils in pits 1,3-Octadiene 1 mm tion of wee 0.2 HO Propor Linalool 0.0 010 100 1000 10,000 100,000 650,000 GC-FID B EAD 1 mV Downloaded from 5 Fig. 1. Z. furfuracea produce two main volatile components, 1,3-octadiene and linalool, yet R. furfuracea only physiologically respond to 1,3-octadiene. Gas chromatography–flame ionization detector (GC-FID) of Z. furfuracea plant cone volatiles is shown at the top with an example male R. furfuracea weevil electro- 0 antenograph detection (EAD) on the bottom. Scale bar, 1 mV for EAD channel. Red arrow denotes a positive physiological response of weevils to 1,3-octadiene that is http://advances.sciencemag.org/ n (mm) sample box ment toward not seen for linalool ( = 10). Weevil response to 1,3-octadiene and lack of response ve –5 to linalool were confirmed with standards (n = 6). Photo credit: Shayla Salzman, Cornell University. evil mo evil We –10 10,000 650,000 Fig. 1), explaining why previous attempts to elicit behavioral re- ng of 1,3-octadiene sponses in R. furfuracea using linalool were unsuccessful (11). Fig. 2. Weevil behavior follows push-pull pollination where they are attracted to lower concentrations of 1,3-octadiene and repelled by higher amounts. Weevil behavioral response to plant volatiles (A) Weevils are preferentially attracted to mid-level amounts of 1,3-octadiene in Because a physiological response does not equate with attraction pitfall tests (shown in fig. S2) and less attracted to more concentrated amounts. on September 14, 2020 and the production of 1,3-octadiene was found to vary over the The proportion of weevils in the bait pit is shown on the y axis. Sequential Bonferonni- course of the day (fig. S1), we analyzed the behavioral response of adjusted P values using an ordinary least squares model are found in table S2. R. furfuracea to different amounts of 1,3-octadiene, covering the (B) Weevils are attracted to and move toward 10,000 ng of 1,3-octadiene and are range of intrinsic plant production. Using pitfall tests where groups repelled and move away from that of 650,000 ng in behavioral arenas (shown in fig. S3). of 4 to 10 weevils are introduced for a period of 30 min to a dilution Significance is determined using an ordinary least squares model. Measurements of 1,3-octadiene in dichloromethane or a control (fig. S2), we show above the gray line show a change in average weevil position toward the that R. furfuracea are positively attracted to 1,3-octadiene and that 1,3- octadiene sample and below the line a shift away from the sample. Individual weevil attraction to increasing amounts of 1,3-octadiene is nonlinear points represent one trial of 4 to 10 weevils in (A) and one trial of ~80 weevils in (B). m (Fig. 2A). Weevils are
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